Abstract
An iron reducing enrichment was obtained from sulfate reducing sludge and was evaluated on the capability of reducing Fe3+ coupled to acetate oxidation in a microbial fuel cell (MFC). Three molar ratios for acetate/Fe3+ were evaluated (2/16, 3.4/27 and 6.9/55 mM). The percentages of Fe3+ reduction were in a range of 80–90, 60–70 and 40–50% for the MFCs at closed circuit for the molar ratios of 2/16, 3.4/27 and 6.9/55 mM, respectively. Acetate consumption was in a range of 80–90% in all cases. The results obtained at closed circuit for current density were: 11.37 mA/m2, 4.5 mA/m2 and 7.37 mA/m2 for the molar ratios of 2/16, 3.4/27 and 6.9/55 mM, respectively. Some microorganisms that were isolated and identified in the MFCs were Azospira oryzae, Cupriavidus metallidurans CH34, Enterobacter bugandensis 247BMC, Citrobacter freundii ATCC8090 and Citrobacter murliniae CDC2970-59, these bacteria have been reported as exoelectrogens in MFC and in MFC involving metals removal but not all of them have been reported to utilize acetate as preferred substrate. The results demonstrate that the isolates can utilize acetate as the sole source of carbon and suggest that Fe3+ reduction was carried out by a combination of different mechanisms (direct contact and redox mediators) utilized by the bacteria identified in the MFC. Storage of the energy generated from the 2/16 mM MFC system arranged in a series of three demonstrated that it is possible to utilize the energy to charge a battery.
Graphic abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altschul SF, Madden TL, Schäffer AA et al (1997) Gapped BLAST and PSI-BLAST: a new generation of proteindatabase search programs. Nuclei Acids Res 25:3389–3402
American Public Health Association (APHA) (2000) Standard methods for examination of water and wastewater. American Public Health Association (APHA), Washington DC
Baranitharan E, Khan MR, Yousuf A et al (2015) Enhanced power generation using controlled inoculum from palm oil mill effluent fed microbial fuel cell. Fuel 143:72–79. https://doi.org/10.1016/j.fuel.2014.11.030
Biancalana Costa R, Gouvea Godoi L, Braga FM et al (2021) Sulfate removal rate and metal recovery as settling precipitates in bioreactors: influence of electron donors. J Hazard Mater 403:123622. https://doi.org/10.1016/j.jhazmat.2020.123622
Dai Q, Zhang S, Liu H et al (2020) Sulfide-mediated azo dye degradation andmicrobial community analysis in a single-chamber air cathode microbial fuel cell. Bioelectrochemistry 131:107349. https://doi.org/10.1016/j.bioelechem.2019.107349
Debabov VG (2008) Electricity from microorganisms. Mikrobiologiya 77(2):149–157. https://doi.org/10.1134/S002626170802001X
Diels L, Van Roy S, Taghavi S, Van Houdt R (2009) From industrial sites to environmental applications with Cupriavidus metallidurans. Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology, 96(2 SPEC. ISS.), p 247–258. https://doi.org/10.1007/s10482-009-9361-4
Doijad S, Imirzalioglu C, Yao Y, Pati NB, Falgenhauer L, Hain T, Foesel BU, Abt B, Overmann J, Mirambo MM, Mshana SE, Chakraborty T (2016) Enterobacter bugandensis sp. nov., isolated from neonatal blood. Int J Syst Evol Microbiol 66(2):968–974. https://doi.org/10.1099/ijsem.0.000821
Espinoza-Tofalos A, Daghio M, González M, Papacchini M, Franzetti A, Seeger M (2018) Toluene degradation by Cupriavidus metallidurans CH34 in nitrate reducing conditions and in bioelectrochemical systems. FEMS Microbiol Lett 365:fny119. https://doi.org/10.1093/femsle/fny119
García-Solares SM, Ordaz A, Monroy-Hermosillo O, Jan-Roblero J (2014) High sulfate reduction efficiency in a UASB using an alternative source of sulfidogenic sludge derived from hydrothermal vent sediments. Appl Biochem Biotechnol 174:2919–2940. https://doi.org/10.1007/s12010-014-1237-z
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows95/98/NT. Nucleic Acids Symp Series 41:95–98
Hassan M, Wei H, Qiu H, Su Y et al (2018) Power generation and pollutants removal from landfill leachate in microbial fuel cell: variation and influence of anodic microbiomes. Bioresour Technol 247:434–442. https://doi.org/10.1016/j.biortech.2017.09.124
Huang J, Zhu N, Cao Y, Peng Y, Wu P, Dong W (2015) Exoelectrogenic bacterium phylogenetically related to Citrobacter freundii, isolated from anodic biofilm of a microbial fuel cell. Appl Biochem Biotechnol 175(4):1879–1891. https://doi.org/10.1007/s12010-014-1418-9
Hunter WJ (2007) An Azospira oryzae (syn Dechlorosoma suillum) strain that reduces selenate and selenite to elemental red selenium. Curr Microbiol 54:376–381. https://doi.org/10.1007/s00284006-0474-y
Kim GT, Webster G, Wimpenny JWT, Kim BH, Kim HJ, Weightman AJ (2006) Bacterial community structure, compartmentalization and activity in a microbial fuel cell. J Appl Microbiol 101(3):698–710. https://doi.org/10.1111/j.1365-2672.2006.02923.x
Kousi P, Remoundaki E, Hatzikioseyian A, Battaglia-Brunet F (2011) Metal precipitation in an ethanol-fed, fixed-bed sulphate-reducing bioreactor. J Hazard Mater 189:677–684
Kumar SS, Malyan SK, Basu S, Bishnoi NR (2017) Syntrophic association and performance of Clostridium, Desulfovibrio, Aeromonas and Tetrathiobacter as anodic biocatalysts for bioelectricity generation in dual chamber microbial fuel cell. Environ Sci Pollut Res 24:16019–16030. https://doi.org/10.1007/s11356-017-9112-4
Liu H, Wang H (2016) Characterization of Fe(III)-reducing enrichment culture and isolation of Fe(III)-reducing bacterium Enterobacter sp. L6 from marine sediment. J Biosci Bioeng 122(1):92–96. https://doi.org/10.1016/j.jbiosc.2015.12.014
Liu L, Lee DJ, Wang A, Ren N, Su A, Lai JY (2016) Isolation of Fe(III)-reducing bacterium, Citrobacter sp. LAR-1, for startup of microbial fuel cell. Int J Hydrogen Energy 41(7):4498–4503. https://doi.org/10.1016/j.ijhydene.2015.07.072
Logan BE, Hamelers B, Rozendal R, Schröder U, Keller J, Freguia S, Aelterman P, Verstraete W, Rabaey K (2006) Microbial fuel cells: methodology and technology. Environ Sci Technol 40(17):5181–5192. https://doi.org/10.1021/es0605016
Lopes SI, Sulistyawati I, Capela M, Lens PN (2007) Low pH (6, 5 and 4) sulfate reduction during the acidification of sucrose under thermophilic (55°C) conditions. Process Biochem 42:580–591
Lovley DR (2006) Bug juice: harvesting electricity with microorganisms. Nat Rev Microbiol 4(7):497–508. https://doi.org/10.1038/nrmicro1442
Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49(2):219–286. https://doi.org/10.1016/S0065-2911(04)49005-5
Mahmoud RH, Samhan FA, Ibrahim MK et al (2021) Formation of electroactive biofilms derived by nanostructured anodes surfaces. Bioprocess Biosyst Eng. https://doi.org/10.1007/s00449-020-02485-4
Martins M, Faleiro ML, Barros RJ, Veríssimo AR, Barreiros MA, Costa MC (2009) Characterization and activity studies of highly heavy metal resistant sulphate-reducing bacteria to be used in acid mine drainage decontamination. J Hazard Mater 166(2–3):706–713. https://doi.org/10.1016/j.jhazmat.2008.11.088
Martins Costa J, Piacentini Rodriguez R, Patrícia Sancinetti G (2017) Removal sulfate and metals Fe+2, Cu+2 and Zn+2 from acid mine drainage in an anaerobic sequential batch reactor. J Environ Chem Eng 5:1985–1989
Martins Costa J, Cappuccio de Castro K, Piacentini Rodriguez R et al (2020) Anaerobic reactors for the treatment of sulphate and metal-rich wastewater: a review. Int J Environ Anal Chem. https://doi.org/10.1080/03067319.2020.1728261
Michaelidou U, Heijne A, Euverink GJW, Hamelers HVM et al (2011) Microbial communities and electrochemical performance of titanium-based anodic electrodes in a microbial fuel cell. Appl Environ Microbiol 77(3):1069–1075. https://doi.org/10.1128/AEM.02912-09
Miran W, Jang J, Nawaz M et al (2017) Mixed sulfate-reducing bacteria-enriched microbial fuel cells for the treatment of wastewater containing copper. Chemosphere 189:134–142. https://doi.org/10.1016/j.chemosphere.2017.09.048
Najib T, Solgi M, Farazmand A et al (2017) Optimization of sulfate removal by sulfate reducing bacteria using response surface methodology and heavy metal removal in a sulfidogenic UASB Reactor. J Environ Chem Eng 5:3256–3265. https://doi.org/10.1016/j.jece.2017.06.016
Nevin KP, Lovley DR (2002) Mechanisms for Fe(III) oxide reduction in sedimentary environments. Geomicrobiol J 19(2):141–159. https://doi.org/10.1080/01490450252864253
Özkaya B, Kaksonen AH, Sahinkaya E, Puhakka JA (2019) Fluidized bed bioreactor for multiple environmental engineering solutions. Water Res 150:452–465. https://doi.org/10.1016/j.watres.2018.11.061
Park HS, Lin S, Voordouw G (2008) Ferric iron reduction by Desulfovibrio vulgaris Hildenborough wild type and energy metabolism mutants. Antonie Van Leeuwenhoek 93(1–2):79–85. https://doi.org/10.1007/s10482-007-9181-3
Rodrigues ICB, Leão VC (2020) Producing electrical energy in microbial fuel cells based on sulphate reduction: a review. Environ Sci Pollut Res 27:36075–36084. https://doi.org/10.1007/s11356-020-09728-7
Sánchez-Andrea I, Sanz JL, Bijmans MFM, Stams AJM (2014) Sulfate reduction at low pH to remediate acid mine drainage. J Hazard Mater 269:98–109
Sharma M, Varanasi JL, Jain P, Dureja P, Lal B, Domínguez-Benetton X, Pant D, Sarma PM (2014) Influence of headspace composition on product diversity by sulphate reducing bacteria biocathode. Bioresour Technol 165:365–371. https://doi.org/10.1016/j.biortech.2014.03.075
Sharma M, Sarma PM, Pant D, Domínguez-Benetton X (2015) Optimization of electrochemical parameters for sulfate-reducing bacteria (SRB) based biocathode. RSC Adv 5:39601–39611. https://doi.org/10.1039/c5ra04120a
Shi Y, Sun K, Qi X, Gao Q (2015) The fabrication of bio-ceramsite for the removal of heavy metals and its toxicity to bacteria. J Wuhan Univ Technol Mater Sci Ed 30(3):649–654. https://doi.org/10.1007/s11595-015-1205-7
Vandamme P, Coenye T (2004) Taxonomy of the genus Cupriavidus: a tale of lost and found. Int J Syst Evol Microbiol 54(6):2285–2289. https://doi.org/10.1099/ijs.0.63247-0
Venkidusami K, Rao Hari A, Megharaj M (2018) Petrophilic, Fe(III) reducing exoelectrogen Citrobacter sp. KVM11, isolated from hydrocarbon fed microbial electrochemical remediation systems. Front Microbiol 9:349. https://doi.org/10.3389/fmicb.2018.00349
Viollier E, Inglett PW, Hunter K et al (2000) The ferrozine method revisited: Fe(II)/ Fe(III) determination in natural waters. Appl Geochem 15:785–790
Wang A, Liu L, Sun D, Ren N, Lee DJ (2010) Isolation of Fe(III)-reducing fermentative bacterium Bacteroides sp. W7 in the anode suspension of a microbial electrolysis cell (MEC). Int J Hydrogen Energy 35:3178–3182. https://doi.org/10.1016/j.ijhydene.2009.12.154
Xu S, Liu H (2011) New exoelectrogen Citrobacter sp. SX-1 isolated from a microbial fuel cell. J Appl Microbiol 111(5):1108–1115. https://doi.org/10.1111/j.1365-2672.2011.05129.x
Xu X, Zhao Q, Wu M, Ding J, Zhang W (2017) Biodegradation of organic matter and anodic microbial communities analysis in sediment microbial fuel cells with/without Fe(III) oxide addition. Bioresour Technol 225:402–408. https://doi.org/10.1016/j.biortech.2016.11.126
Zhang D, Li Z, Zhang C, Zhou X, Xiao Z, Awata T, Katayama A (2017) Phenol-degrading anode biofilm with high coulombic efficiency in graphite electrodes microbial fuel cell. J Biosci Bioeng 123(3):364–369. https://doi.org/10.1016/j.jbiosc.2016.10.010
Zhuang L, Zhou S, Yuan Y, Liu T et al (2011) Development of Enterobacter aerogenes fuel cells: from in situ biohydrogen oxidization to direct electroactive biofilm. Bioresour Technol 102:284–289. https://doi.org/10.1016/j.biortech.2010.06.038
Acknowledgements
The authors are grateful for the financial support provided by Secretaría de Investigación y Posgrado (SIP) Instituto Politécnico Nacional 20201126, recipient: G – B, C., and the graduate scholarship (CONACYT) awarded to K. B-V.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there are no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Becerril-Varela, K., Serment-Guerrero, J.H., Manzanares-Leal, G.L. et al. Generation of electrical energy in a microbial fuel cell coupling acetate oxidation to Fe3+ reduction and isolation of the involved bacteria. World J Microbiol Biotechnol 37, 104 (2021). https://doi.org/10.1007/s11274-021-03077-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-021-03077-4